Different origins of paralogues of salmonid TNR1 and TNFR2: characterisation and expression analysis of four TNF receptor genes in rainbow trout Oncorhynchus mykiss

Suhee Hong, Ting-Yu Wang, Christopher J. Secombes (Corresponding Author), Tiehui Wang (Corresponding Author)

Research output: Contribution to journalArticle

Abstract

Mammalian TNFR1 and TNFR2 bind TNFα and TNFβ, and provide key communication signals to a variety of cell types during development and immune responses that are crucial for cell survival, proliferation and apoptosis. In teleost fish TNFβ is absent but TNFα has been expanded by the third whole genome duplication (3R WGD) and again by a 4R WGD in some lineages, leading to the four TNFα paralogues known in salmonids. Two paralogues for each of TNFR1 and TNFR2 have been cloned in rainbow trout in this study and are present in other salmonid genomes. Whilst the TNFR2 paralogues were generated via the 4R salmonid WGD, the TNFR1 paralogues arose from a local en bloc duplication. Functional diversification of TNFR paralogues was evidenced by differential gene expression and modulation, upstream ATGs affecting translation, ATTTA motifs in the 3′-UTR regulating mRNA stability, and post-translational modification by N-glycosylation. Trout TNFR are highly expressed in immune tissues/organs, and other tissues, in a gene- and tissue-specific manner. Furthermore, their expression is differentially modulated by PAMPs and cytokines in a cell type- and stimulant-specific manner. Such findings suggest an important role of the TNF/TNFR axis in the immune response and other physiological processes in fish.

Original languageEnglish
Article number103403
Number of pages12
JournalDevelopmental and Comparative Immunology
Volume99
Early online date29 May 2019
DOIs
Publication statusE-pub ahead of print - 29 May 2019

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Receptors, Tumor Necrosis Factor, Type II
Receptors, Tumor Necrosis Factor, Type I
Tumor Necrosis Factor Receptors
Oncorhynchus mykiss
Fishes
Genome
Physiological Phenomena
Genes
Salmonidae
Trout
RNA Stability
3' Untranslated Regions
Post Translational Protein Processing
Glycosylation
Cell Survival
Communication
Cell Proliferation
Apoptosis
Cytokines
Gene Expression

Keywords

  • rainbow trout
  • TNFR1
  • TNFR2
  • Paralogues
  • en bloc duplication
  • gene expression
  • Rainbow trout
  • Gene expression
  • MOLECULAR CHARACTERIZATION
  • PROTEIN
  • ALPHA
  • FUNCTIONAL-CHARACTERIZATION
  • TUMOR-NECROSIS-FACTOR
  • EVOLUTION
  • CLONING
  • FISH
  • SUPERFAMILY
  • CELL-LINE

ASJC Scopus subject areas

  • Immunology
  • Developmental Biology

Cite this

@article{f29a14c1443543eb90104f1dd8dac685,
title = "Different origins of paralogues of salmonid TNR1 and TNFR2: characterisation and expression analysis of four TNF receptor genes in rainbow trout Oncorhynchus mykiss",
abstract = "Mammalian TNFR1 and TNFR2 bind TNFα and TNFβ, and provide key communication signals to a variety of cell types during development and immune responses that are crucial for cell survival, proliferation and apoptosis. In teleost fish TNFβ is absent but TNFα has been expanded by the third whole genome duplication (3R WGD) and again by a 4R WGD in some lineages, leading to the four TNFα paralogues known in salmonids. Two paralogues for each of TNFR1 and TNFR2 have been cloned in rainbow trout in this study and are present in other salmonid genomes. Whilst the TNFR2 paralogues were generated via the 4R salmonid WGD, the TNFR1 paralogues arose from a local en bloc duplication. Functional diversification of TNFR paralogues was evidenced by differential gene expression and modulation, upstream ATGs affecting translation, ATTTA motifs in the 3′-UTR regulating mRNA stability, and post-translational modification by N-glycosylation. Trout TNFR are highly expressed in immune tissues/organs, and other tissues, in a gene- and tissue-specific manner. Furthermore, their expression is differentially modulated by PAMPs and cytokines in a cell type- and stimulant-specific manner. Such findings suggest an important role of the TNF/TNFR axis in the immune response and other physiological processes in fish.",
keywords = "rainbow trout, TNFR1, TNFR2, Paralogues, en bloc duplication, gene expression, Rainbow trout, Gene expression, MOLECULAR CHARACTERIZATION, PROTEIN, ALPHA, FUNCTIONAL-CHARACTERIZATION, TUMOR-NECROSIS-FACTOR, EVOLUTION, CLONING, FISH, SUPERFAMILY, CELL-LINE",
author = "Suhee Hong and Ting-Yu Wang and Secombes, {Christopher J.} and Tiehui Wang",
note = "SH was financially supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (No. 2017R1A2B2011167). T-YW was financially supported by the Ministry of Science and Technology, Taiwan (MOST 107-2917-I-564-019). TW received funding from the Marine Alliance for Science and Technology for Scotland (MASTS), a pooling initiative funded by the Scottish Funding Council (grant reference HR09011).",
year = "2019",
month = "5",
day = "29",
doi = "10.1016/j.dci.2019.103403",
language = "English",
volume = "99",
journal = "Developmental and Comparative Immunology",
issn = "0145-305X",
publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Different origins of paralogues of salmonid TNR1 and TNFR2

T2 - characterisation and expression analysis of four TNF receptor genes in rainbow trout Oncorhynchus mykiss

AU - Hong, Suhee

AU - Wang, Ting-Yu

AU - Secombes, Christopher J.

AU - Wang, Tiehui

N1 - SH was financially supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (No. 2017R1A2B2011167). T-YW was financially supported by the Ministry of Science and Technology, Taiwan (MOST 107-2917-I-564-019). TW received funding from the Marine Alliance for Science and Technology for Scotland (MASTS), a pooling initiative funded by the Scottish Funding Council (grant reference HR09011).

PY - 2019/5/29

Y1 - 2019/5/29

N2 - Mammalian TNFR1 and TNFR2 bind TNFα and TNFβ, and provide key communication signals to a variety of cell types during development and immune responses that are crucial for cell survival, proliferation and apoptosis. In teleost fish TNFβ is absent but TNFα has been expanded by the third whole genome duplication (3R WGD) and again by a 4R WGD in some lineages, leading to the four TNFα paralogues known in salmonids. Two paralogues for each of TNFR1 and TNFR2 have been cloned in rainbow trout in this study and are present in other salmonid genomes. Whilst the TNFR2 paralogues were generated via the 4R salmonid WGD, the TNFR1 paralogues arose from a local en bloc duplication. Functional diversification of TNFR paralogues was evidenced by differential gene expression and modulation, upstream ATGs affecting translation, ATTTA motifs in the 3′-UTR regulating mRNA stability, and post-translational modification by N-glycosylation. Trout TNFR are highly expressed in immune tissues/organs, and other tissues, in a gene- and tissue-specific manner. Furthermore, their expression is differentially modulated by PAMPs and cytokines in a cell type- and stimulant-specific manner. Such findings suggest an important role of the TNF/TNFR axis in the immune response and other physiological processes in fish.

AB - Mammalian TNFR1 and TNFR2 bind TNFα and TNFβ, and provide key communication signals to a variety of cell types during development and immune responses that are crucial for cell survival, proliferation and apoptosis. In teleost fish TNFβ is absent but TNFα has been expanded by the third whole genome duplication (3R WGD) and again by a 4R WGD in some lineages, leading to the four TNFα paralogues known in salmonids. Two paralogues for each of TNFR1 and TNFR2 have been cloned in rainbow trout in this study and are present in other salmonid genomes. Whilst the TNFR2 paralogues were generated via the 4R salmonid WGD, the TNFR1 paralogues arose from a local en bloc duplication. Functional diversification of TNFR paralogues was evidenced by differential gene expression and modulation, upstream ATGs affecting translation, ATTTA motifs in the 3′-UTR regulating mRNA stability, and post-translational modification by N-glycosylation. Trout TNFR are highly expressed in immune tissues/organs, and other tissues, in a gene- and tissue-specific manner. Furthermore, their expression is differentially modulated by PAMPs and cytokines in a cell type- and stimulant-specific manner. Such findings suggest an important role of the TNF/TNFR axis in the immune response and other physiological processes in fish.

KW - rainbow trout

KW - TNFR1

KW - TNFR2

KW - Paralogues

KW - en bloc duplication

KW - gene expression

KW - Rainbow trout

KW - Gene expression

KW - MOLECULAR CHARACTERIZATION

KW - PROTEIN

KW - ALPHA

KW - FUNCTIONAL-CHARACTERIZATION

KW - TUMOR-NECROSIS-FACTOR

KW - EVOLUTION

KW - CLONING

KW - FISH

KW - SUPERFAMILY

KW - CELL-LINE

UR - http://www.mendeley.com/research/different-origins-paralogues-salmonid-tnr1-tnfr2-characterisation-expression-analysis-four-tnf-recep

U2 - 10.1016/j.dci.2019.103403

DO - 10.1016/j.dci.2019.103403

M3 - Article

VL - 99

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

SN - 0145-305X

M1 - 103403

ER -